Prophage excision activates listeria competence genes that promote phagosomal escape and virulence

Cell

Volumn 150, Issue 4, 2012, Pages 792-802

  Rabinovich, Lev ^a   Sigal, Nadejda ^a   Borovok, Ilya ^a   Nir Paz, Ran ^b   Herskovits, Anat A ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; COMK BACTERIAL GENE; COMPETENCE BACTERIAL GENE; LISTERIA MONOCYTOGENES; MACROPHAGE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROGENY; PROPHAGE; VIRION;

EID: 84865240356     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.06.036     Document Type: Article

References (53)

1. R.M. Berka, J. Hahn, M. Albano, I. Draskovic, M. Persuh, X. Cui, A. Sloma, W. Widner, and D. Dubnau Microarray analysis of the Bacillus subtilis K-state: genome-wide expression changes dependent on ComK Mol. Microbiol. 43 2002 1331 1345 (Pubitemid 34304547)
2. C.L. Birmingham, V. Canadien, N.A. Kaniuk, B.E. Steinberg, D.E. Higgins, and J.H. Brumell Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles Nature 451 2008 350 354
3. E. Borezee, T. Msadek, L. Durant, and P. Berche Identification in Listeria monocytogenes of MecA, a homologue of the Bacillus subtilis competence regulatory protein J. Bacteriol. 182 2000 5931 5934
4. E. Borezée, E. Pellegrini, J.L. Beretti, and P. Berche SvpA, a novel surface virulence-associated protein required for intracellular survival of Listeria monocytogenes Microbiology 147 2001 2913 2923 (Pubitemid 33076980)
5. H. Brüssow, C. Canchaya, and W.D. Hardt Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion Microbiol. Mol. Biol. Rev. 68 2004 560 602 (Pubitemid 39238283)
6. I. Chen, and D. Dubnau DNA uptake during bacterial transformation Nat. Rev. Microbiol. 2 2004 241 249 (Pubitemid 39490085)
7. J.P. Claverys, M. Prudhomme, and B. Martin Induction of competence regulons as a general response to stress in gram-positive bacteria Annu. Rev. Microbiol. 60 2006 451 475 (Pubitemid 44627957)
8. P. Cossart, M.F. Vicente, J. Mengaud, F. Baquero, J.C. Perez-Diaz, and P. Berche Listeriolysin O is essential for virulence of Listeria monocytogenes: direct evidence obtained by gene complementation Infect. Immun. 57 1989 3629 3636 (Pubitemid 19259901)
9. J. Dorscht, J. Klumpp, R. Bielmann, M. Schmelcher, Y. Born, M. Zimmer, R. Calendar, and M.J. Loessner Comparative genome analysis of Listeria bacteriophages reveals extensive mosaicism, programmed translational frameshifting, and a novel prophage insertion site J. Bacteriol. 191 2009 7206 7215
10. D. Dubnau DNA uptake in bacteria Annu. Rev. Microbiol. 53 1999 217 244 (Pubitemid 29503731)
11. R. Fronzes, P.J. Christie, and G. Waksman The structural biology of type IV secretion systems Nat. Rev. Microbiol. 7 2009 703 714
12. I.J. Glomski, M.M. Gedde, A.W. Tsang, J.A. Swanson, and D.A. Portnoy The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells J. Cell Biol. 156 2002 1029 1038 (Pubitemid 34839852)
13. J.W. Golden, S.J. Robinson, and R. Haselkorn Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena Nature 314 1985 419 423 (Pubitemid 15145581)
14. A. Gründling, M.D. Gonzalez, and D.E. Higgins Requirement of the Listeria monocytogenes broad-range phospholipase PC-PLC during infection of human epithelial cells J. Bacteriol. 185 2003 6295 6307 (Pubitemid 37305529)
15. J. Hahn, B. Maier, B.J. Haijema, M. Sheetz, and D. Dubnau Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis Cell 122 2005 59 71 (Pubitemid 40977940)
16. L.W. Hamoen, A.F. Van Werkhoven, J.J. Bijlsma, D. Dubnau, and G. Venema The competence transcription factor of Bacillus subtilis recognizes short A/T-rich sequences arranged in a unique, flexible pattern along the DNA helix Genes Dev. 12 1998 1539 1550 (Pubitemid 28243638)
17. M. Hamon, H. Bierne, and P. Cossart Listeria monocytogenes: a multifaceted model Nat. Rev. Microbiol. 4 2006 423 434 (Pubitemid 43771862)
18. A.A. Herskovits, V. Auerbuch, and D.A. Portnoy Bacterial ligands generated in a phagosome are targets of the cytosolic innate immune system PLoS Pathog. 3 2007 e51
19. D.A. Hodgson Generalized transduction of serotype 1/2 and serotype 4b strains of Listeria monocytogenes Mol. Microbiol. 35 2000 312 323 (Pubitemid 30055228)
20. A.D. Johnson, A.R. Poteete, G. Lauer, R.T. Sauer, G.K. Ackers, and M. Ptashne lambda Repressor and cro - components of an efficient molecular switch Nature 294 1981 217 223
21. S. Kathariou, P. Metz, H. Hof, and W. Goebel Tn916-induced mutations in the hemolysin determinant affecting virulence of Listeria monocytogenes J. Bacteriol. 169 1987 1291 1297 (Pubitemid 17043401)
22. J.E. Kirby, J.E. Trempy, and S. Gottesman Excision of a P4-like cryptic prophage leads to Alp protease expression in Escherichia coli J. Bacteriol. 176 1994 2068 2081 (Pubitemid 24103558)
23. L. Kroos, B. Kunkel, and R. Losick Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor Science 243 1989 526 529 (Pubitemid 19048751)
24. B. Kunkel, R. Losick, and P. Stragier The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene Genes Dev. 4 1990 525 535
25. P. Lauer, M.Y. Chow, M.J. Loessner, D.A. Portnoy, and R. Calendar Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors J. Bacteriol. 184 2002 4177 4186 (Pubitemid 34774298)
26. J.H. Leber, G.T. Crimmins, S. Raghavan, N.P. Meyer-Morse, J.S. Cox, and D.A. Portnoy Distinct TLR- and NLR-mediated transcriptional responses to an intracellular pathogen PLoS Pathog. 4 2008 e6
27. J.W. Little, and D.W. Mount The SOS regulatory system of Escherichia coli Cell 29 1982 11 22 (Pubitemid 12027667)
28. M.J. Loessner, R.B. Inman, P. Lauer, and R. Calendar Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution Mol. Microbiol. 35 2000 324 340 (Pubitemid 30055229)
29. M.J. Loessner, G. Wendlinger, and S. Scherer Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes Mol. Microbiol. 16 1995 1231 1241
30. H. Maamar, and D. Dubnau Bistability in the Bacillus subtilis K-state (competence) system requires a positive feedback loop Mol. Microbiol. 56 2005 615 624 (Pubitemid 40562357)
31. M.D. Miner, G.C. Port, and N.E. Freitag Functional impact of mutational activation on the Listeria monocytogenes central virulence regulator PrfA Microbiology 154 2008 3579 3589
32. M. O'Riordan, C.H. Yi, R. Gonzales, K.D. Lee, and D.A. Portnoy Innate recognition of bacteria by a macrophage cytosolic surveillance pathway Proc. Natl. Acad. Sci. USA 99 2002 13861 13866 (Pubitemid 35215471)
33. D.A. Portnoy, P.S. Jacks, and D.J. Hinrichs Role of hemolysin for the intracellular growth of Listeria monocytogenes J. Exp. Med. 167 1988 1459 1471
34. M.T. Ripio, K. Brehm, M. Lara, M. Suárez, and J.A. Vázquez-Boland Glucose-1-phosphate utilization by Listeria monocytogenes is PrfA dependent and coordinately expressed with virulence factors J. Bacteriol. 179 1997 7174 7180 (Pubitemid 27492506)
35. J. Scott, P. Thompson-Mayberry, S. Lahmamsi, C.J. King, and W.M. McShan Phage-associated mutator phenotype in group A streptococcus J. Bacteriol. 190 2008 6290 6301
36. G.A. Smith, H. Marquis, S. Jones, N.C. Johnston, D.A. Portnoy, and H. Goldfine The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread Infect. Immun. 63 1995 4231 4237
37. P. Stragier, B. Kunkel, L. Kroos, and R. Losick Chromosomal rearrangement generating a composite gene for a developmental transcription factor Science 243 1989 507 512 (Pubitemid 19048749)
38. L.G. Tilney, and D.A. Portnoy Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes J. Cell Biol. 109 1989 1597 1608
39. D. van Sinderen, A. Luttinger, L. Kong, D. Dubnau, G. Venema, and L. Hamoen comK encodes the competence transcription factor, the key regulatory protein for competence development in Bacillus subtilis Mol. Microbiol. 15 1995 455 462
40. G. Wendlinger, M.J. Loessner, and S. Scherer Bacteriophage receptors on Listeria monocytogenes cells are the N-acetylglucosamine and rhamnose substituents of teichoic acids or the peptidoglycan itself Microbiology 142 1996 985 992 (Pubitemid 26139373)
41. R. Zink, and M.J. Loessner Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis Appl. Environ. Microbiol. 58 1992 296 302
42. Bergmann, B., Raffelsbauer, D., Kuhn, M., Goetz, M., Hom, S., and Goebel, W. (2002). InlA- but not InlB-mediated internalization of Listeria monocytogenes by non-phagocytic mammalian cells needs the support of other internalins. Mol. Microbiol. 43, 557-570. (Pubitemid 34597253)
43. Dorscht, J., Klumpp, J., Bielmann, R., Schmelcher, M., Born, Y., Zimmer, M., Calendar, R., and Loessner, M.J. (2009). Comparative genome analysis of Listeria bacteriophages reveals extensive mosaicism, programmed translational frameshifting, and a novel prophage insertion site. J. Bacteriol. 191, 7206-7215.
44. Geoffroy, C., Raveneau, J., Beretti, J.L., Lecroisey, A., Vazquez-Boland, J.A., Alouf, J.E., and Berche, P. (1991). Purification and characterization of an extracellular 29-kilodalton phospholipase C from Listeria monocytogenes. Infect. Immun. 59, 2382-2388.
45. Glomski, I.J., Gedde, M.M., Tsang, A.W., Swanson, J.A., and Portnoy, D.A. (2002). The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J. Cell Biol. 156, 1029-1038. (Pubitemid 34839852)
46. Herskovits, A.A., Auerbuch, V., and Portnoy, D.A. (2007). Bacterial ligands generated in a phagosome are targets of the cytosolic innate immune system. PLoS Pathog. 3, e51.
47. Lauer, P., Chow, M.Y., Loessner, M.J., Portnoy, D.A., and Calendar, R. (2002). Construction, characterization, and use of two Listeria monocytogenes site-specific phage integration vectors. J. Bacteriol. 184, 4177-4186. (Pubitemid 34774298)
48. Lauer, P., Hanson, B., Lemmens, E.E., Liu, W., Luckett, W.S., Leong, M.L., Allen, H.E., Skoble, J., Bahjat, K.S., Freitag, N.E., et al. (2008). Constitutive activation of the PrfA regulon enhances the potency of vaccines based on live-attenuated and killed but metabolically active Listeria monocytogenes strains. Infect. Immun. 76, 3742-3753.
49. Leimeister-Wächter, M., Goebel, W., and Chakraborty, T. (1989). Mutations affecting hemolysin production in Listeria monocytogenes located outside the listeriolysin gene. FEMS Microbiol. Lett. 53, 23-29. (Pubitemid 19285740)
50. Miner, M.D., Port, G.C., and Freitag, N.E. (2008). Functional impact of mutational activation on the Listeria monocytogenes central virulence regulator PrfA. Microbiology 154, 3579-3589.
51. Simon, R., Priefer, U., and Pühler, A. (1983). A broad host range mobilization system for in vitro genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1, 784-791. (Pubitemid 14239484)
52. Susanna, K.A., Mironczuk, A.M., Smits, W.K., Hamoen, L.W., and Kuipers, O.P. (2007). A single, specific thymine mutation in the ComK-binding site severely decreases binding and transcription activation by the competence transcription factor ComK of Bacillus subtilis. J. Bacteriol. 189, 4718-4728. (Pubitemid 47025583)
53. Yeung, P.S., Zagorski, N., and Marquis, H. (2005). The metalloprotease of Listeria monocytogenes controls cell wall translocation of the broad-range phospholipase C. J. Bacteriol. 187, 2601-2608. (Pubitemid 40490365)